Department of Biology, Trinity Western University, Langley, British Columbia, Canada.
International Collaboration on Repair Discoveries (ICORD), University of British Columbia, Vancouver, British Columbia, Canada.
PLoS One. 2016 Oct 31;11(10):e0165162. doi: 10.1371/journal.pone.0165162. eCollection 2016.
"Rods and rings" (RR) and loukoumasomes are similarly shaped, subcellular macromolecular structures with as yet unknown function. RR, so named because of their shape, are formed in response to inhibition in the GTP or CTP synthetic pathways and are highly enriched in the two key enzymes of the nucleotide synthetic pathway. Loukoumasomes also occur as linear and toroidal bodies and were initially inferred to be the same as RR, largely due to their shared shape and size and the fact that it was unclear if they shared the same subcomponents. In human retinoblastoma tissue and cells we have observed toroidal, perinuclear, macromolecular structures of similar size and antigenicity to those previously reported in neurons (neuronal-loukoumasomes). To further characterize the subcomponents of the retinal-loukoumasomes, confocal analysis following immunocytochemical staining for alpha-tubulin, beta-III tubulin and detyrosinated tubulin was performed. These studies indicate that retinal-loukoumasomes are enriched for beta-III tubulin and other tubulins associated with microtubules. Immunofluorescence together with the in situ proximity ligation assay (PLA), confirmed that beta-III tubulin colocalized with detyrosinated tubulin within loukoumasomes. Our results indicate that these tissues contain only loukoumasomes because these macromolecular structures are immunoreactive with an anti-tubulin antibody but are not recognized by the prototype anti-RR/inosine monophosphate dehydrogenase (IMPDH) antibody (It2006). To further compare the RR and retinal-loukoumasomes, retinoblastoma cells were exposed to the IMPDH-inhibitor ribavirin, a drug known to induce the formation of RR. In contrast to RR, the production of retinal-loukoumasomes was unaffected. Coimmunostaining of Y79 cells for beta-III tubulin and IMPDH indicate that these cells, when treated with ribavirin, can contain both retinal-loukoumasomes and RR and that these structures are antigenically distinct. Subcellular fractionation studies indicate that ribavirin increased the RR subcomponent, IMPDH, in the nuclear fraction of Y79 cells from 21.3 ± 5.8% (0 mM ribavirin) to 122.8 ± 7.9% (1 mM ribavirin) while the subcellular localization of the retinal-loukoumasome subcomponent tubulin went unaltered. Further characterization of retinal-loukoumasomes in retinoblastoma cells reveals that they are intimately associated with lamin folds within the nuclear envelope. Using immunofluorescence and the in situ PLA in this cell type, we have observed colocalization of beta-III tubulin with MAP2. As MAP2 is a microtubule-associated protein implicated in microtubule crosslinking, this supports a role for microtubule crosslinkers in the formation of retinal-loukoumasomes. Together, these results suggest that loukoumasomes and RR are distinct subcellular macromolecular structures, formed by different cellular processes and that there are other loukoumasome-like structures within retinal tissues and cells.
“棒状体和环体”(RR)和loukoumasomes 具有相似的形状,是具有未知功能的细胞内大分子结构。RR 因其形状而得名,是在 GTP 或 CTP 合成途径受到抑制时形成的,并且在核苷酸合成途径的两个关键酶中高度富集。loukoumasomes 也呈现线性和环形体,最初推断它们与 RR 相同,主要是因为它们具有相似的形状和大小,而且不清楚它们是否共享相同的亚成分。在人视网膜母细胞瘤组织和细胞中,我们观察到了类似大小和抗原性的核周、大分子结构,与神经元中报道的(神经元-loukoumasomes)相似。为了进一步表征视网膜-loukoumasomes 的亚成分,我们对 alpha-tubulin、beta-III tubulin 和去酪氨酸化 tubulin 进行免疫细胞化学染色后的共聚焦分析。这些研究表明,视网膜-loukoumasomes 富含 beta-III tubulin 和其他与微管相关的微管蛋白。免疫荧光结合原位邻近连接分析(PLA)证实,beta-III tubulin 与 loukoumasomes 内的去酪氨酸化 tubulin 共定位。我们的结果表明,这些组织仅包含 loukoumasomes,因为这些大分子结构对微管蛋白抗体具有免疫反应性,但不能被原型抗 RR/肌苷单磷酸脱氢酶(IMPDH)抗体(It2006)识别。为了进一步比较 RR 和视网膜-loukoumasomes,视网膜母细胞瘤细胞暴露于 IMPDH 抑制剂利巴韦林中,利巴韦林是一种已知能诱导 RR 形成的药物。与 RR 相反,视网膜-loukoumasomes 的产生不受影响。Y79 细胞的 beta-III tubulin 和 IMPDH 共免疫染色表明,用利巴韦林处理这些细胞时,它们可以同时包含视网膜-loukoumasomes 和 RR,并且这些结构具有不同的抗原性。亚细胞分级研究表明,利巴韦林使 Y79 细胞核部分的 RR 亚成分,IMPDH,从 21.3±5.8%(0 mM 利巴韦林)增加到 122.8±7.9%(1 mM 利巴韦林),而视网膜-loukoumasome 亚成分 tubulin 的亚细胞定位保持不变。对视网膜母细胞瘤细胞中视网膜-loukoumasomes 的进一步表征表明,它们与核膜中的核纤层褶皱密切相关。在这种细胞类型中,我们使用免疫荧光和原位 PLA 观察到 beta-III tubulin 与 MAP2 的共定位。由于 MAP2 是一种与微管相关的蛋白质,与微管交联有关,这支持微管交联剂在视网膜-loukoumasomes 形成中的作用。总之,这些结果表明,loukoumasomes 和 RR 是不同的细胞内大分子结构,由不同的细胞过程形成,并且在视网膜组织和细胞中存在其他 loukoumasome 样结构。